Trophic interactions between predatory protists and pathogen-suppressive bacteria impact plant health

Sai Guo; Chengyuan Tao; Alexandre Jousset; Wu Xiong; Zhe Wang; Zongzhuan Shen; Beibei Wang; Zhihui Xu; Zhilei Gao; Shanshan Liu; Rong Li; Yunze Ruan; Qirong Shen; George A. Kowalchuk; Stefan Geisen

doi:10.1038/s41396-022-01244-5

Trophic interactions between predatory protists and pathogen-suppressive bacteria impact plant health

Sai Guo, Chengyuan Tao, Alexandre Jousset, Wu Xiong, Zhe Wang, Zongzhuan Shen, Beibei Wang, Zhihui Xu, Zhilei Gao, Shanshan Liu, Rong Li^*, Yunze Ruan, Qirong Shen, George A. Kowalchuk, Stefan Geisen

^*Corresponding author for this work

NIOO - Terrestrial Ecology (TE)

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

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Abstract

Plant health is strongly impacted by beneficial and pathogenic plant microbes, which are themselves structured by resource inputs. Organic fertilizer inputs may thus offer a means of steering soil-borne microbes, thereby affecting plant health. Concurrently, soil microbes are subject to top-down control by predators, particularly protists. However, little is known regarding the impact of microbiome predators on plant health-influencing microbes and the interactive links to plant health. Here, we aimed to decipher the importance of predator-prey interactions in influencing plant health. To achieve this goal, we investigated soil and root-associated microbiomes (bacteria, fungi and protists) over nine years of banana planting under conventional and organic fertilization regimes differing in Fusarium wilt disease incidence. We found that the reduced disease incidence and improved yield associated with organic fertilization could be best explained by higher abundances of protists and pathogen-suppressive bacteria (e.g. Bacillus spp.). The pathogen-suppressive actions of predatory protists and Bacillus spp. were mainly determined by their interactions that increased the relative abundance of secondary metabolite Q genes (e.g. nonribosomal peptide synthetase gene) within the microbiome. In a subsequent microcosm assay, we tested the interactions between predatory protists and pathogen-suppressive Bacillus spp. that showed strong improvements in plant defense. Our study shows how protistan predators stimulate disease-suppressive bacteria in the plant microbiome, ultimately enhancing plant health and yield. Thus, we suggest a new biological model useful for improving sustainable agricultural practices that is based on complex interactions between different domains of life.

Original language	English
Pages (from-to)	1932-1943
Number of pages	12
Journal	ISME Journal
Volume	16
Issue number	8
DOIs	https://doi.org/10.1038/s41396-022-01244-5
Publication status	Published - 2022

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title = "Trophic interactions between predatory protists and pathogen-suppressive bacteria impact plant health",

abstract = "Plant health is strongly impacted by beneficial and pathogenic plant microbes, which are themselves structured by resource inputs. Organic fertilizer inputs may thus offer a means of steering soil-borne microbes, thereby affecting plant health. Concurrently, soil microbes are subject to top-down control by predators, particularly protists. However, little is known regarding the impact of microbiome predators on plant health-influencing microbes and the interactive links to plant health. Here, we aimed to decipher the importance of predator-prey interactions in influencing plant health. To achieve this goal, we investigated soil and root-associated microbiomes (bacteria, fungi and protists) over nine years of banana planting under conventional and organic fertilization regimes differing in Fusarium wilt disease incidence. We found that the reduced disease incidence and improved yield associated with organic fertilization could be best explained by higher abundances of protists and pathogen-suppressive bacteria (e.g. Bacillus spp.). The pathogen-suppressive actions of predatory protists and Bacillus spp. were mainly determined by their interactions that increased the relative abundance of secondary metabolite Q genes (e.g. nonribosomal peptide synthetase gene) within the microbiome. In a subsequent microcosm assay, we tested the interactions between predatory protists and pathogen-suppressive Bacillus spp. that showed strong improvements in plant defense. Our study shows how protistan predators stimulate disease-suppressive bacteria in the plant microbiome, ultimately enhancing plant health and yield. Thus, we suggest a new biological model useful for improving sustainable agricultural practices that is based on complex interactions between different domains of life.",

author = "Sai Guo and Chengyuan Tao and Alexandre Jousset and Wu Xiong and Zhe Wang and Zongzhuan Shen and Beibei Wang and Zhihui Xu and Zhilei Gao and Shanshan Liu and Rong Li and Yunze Ruan and Qirong Shen and Kowalchuk, {George A.} and Stefan Geisen",

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T1 - Trophic interactions between predatory protists and pathogen-suppressive bacteria impact plant health

AU - Guo, Sai

AU - Tao, Chengyuan

AU - Jousset, Alexandre

AU - Xiong, Wu

AU - Wang, Zhe

AU - Shen, Zongzhuan

AU - Wang, Beibei

AU - Xu, Zhihui

AU - Gao, Zhilei

AU - Liu, Shanshan

AU - Li, Rong

AU - Ruan, Yunze

AU - Shen, Qirong

AU - Kowalchuk, George A.

AU - Geisen, Stefan

N1 - 7439, TE

PY - 2022

Y1 - 2022

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AB - Plant health is strongly impacted by beneficial and pathogenic plant microbes, which are themselves structured by resource inputs. Organic fertilizer inputs may thus offer a means of steering soil-borne microbes, thereby affecting plant health. Concurrently, soil microbes are subject to top-down control by predators, particularly protists. However, little is known regarding the impact of microbiome predators on plant health-influencing microbes and the interactive links to plant health. Here, we aimed to decipher the importance of predator-prey interactions in influencing plant health. To achieve this goal, we investigated soil and root-associated microbiomes (bacteria, fungi and protists) over nine years of banana planting under conventional and organic fertilization regimes differing in Fusarium wilt disease incidence. We found that the reduced disease incidence and improved yield associated with organic fertilization could be best explained by higher abundances of protists and pathogen-suppressive bacteria (e.g. Bacillus spp.). The pathogen-suppressive actions of predatory protists and Bacillus spp. were mainly determined by their interactions that increased the relative abundance of secondary metabolite Q genes (e.g. nonribosomal peptide synthetase gene) within the microbiome. In a subsequent microcosm assay, we tested the interactions between predatory protists and pathogen-suppressive Bacillus spp. that showed strong improvements in plant defense. Our study shows how protistan predators stimulate disease-suppressive bacteria in the plant microbiome, ultimately enhancing plant health and yield. Thus, we suggest a new biological model useful for improving sustainable agricultural practices that is based on complex interactions between different domains of life.

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DO - 10.1038/s41396-022-01244-5

M3 - Article

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SN - 1751-7362

VL - 16

SP - 1932

EP - 1943

JO - ISME Journal

JF - ISME Journal

IS - 8

ER -

Trophic interactions between predatory protists and pathogen-suppressive bacteria impact plant health

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